Trophic relationships and mercury biomagnification in Brazilian tropical coastal food webs
Tatiana Lemos Bisia,b,c*, Gilles Lepointd, Alexandre de Freitas Azevedob, Paulo Renato
Dornelesb,c, Leonardo Flache, Krishna Dasd, Olaf Malmc, José Lailson-Britob
a
Programa de Pós-Graduação em Ecologia, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, 21941-
900, Brazil
b
Aquatic Mammal and Bioindicator Laboratory (MAQUA), School of Oceanography, University of Rio de
Janeiro State (UERJ), Rio de Janeiro, 20550-013, Brazil
c
Radioisotope Laboratory, Biophysics Institute, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro,
21941-900, Brazil
d
Laboratory for Oceanology, MARE Centre, University of Liege, Liege, B-4000, Belgium
e
Projeto Boto cinza, Mangaratiba, RJ, 23860-000, Brazil
ABSTRACT
The present study investigated trophic relationships and mercury flow through food
webs of three tropical coastal ecosystems: Guanabara, Sepetiba and Ilha Grande bays. The
investigation was carried out through carbon and nitrogen stable isotopes (δ13C, δ15N) and
total mercury (THg) determination in muscle from 35 species, including crustacean,
cephalopod, fish and dolphin species. Detritivorous species showed the lowest average δ15N
values in all bays. These species were 13C enriched in Sepetiba and Ilha Grande bays,
suggesting the presence of 13C enriched macroalgae in their diet. The highest mean δ15N
values were found in fish and benthic invertebrate feeders, as well as in species presenting
demerso-pelagic feeding habit. The carbon and nitrogen isotopic findings showed different
trophic relationship in food webs from Sepetiba, Guanabara and Ilha Grande bays. Guanabara
Bay showed to be depleted in δ15N compared to both Sepetiba and Ilha Grande bays. The
*Corresponding author. Universidade Federal do Rio de Janeiro, Instituto de Biofísica, Laboratório de
Radioisótopos, Rio de Janeiro, 21941-900, RJ, Brazil Tel.: +55 21 25615339; Fax: +55 21 22808193
E-mail address: tbisi@yahoo.com.br (T.L. Bisi)
2
latter finding suggests substantial contribution of atmospheric nitrogen fixation by
cyanobacteria. A positive linear relationship was found between log THg concentrations and
δ15N values for Guanabara and Ilha Grande bays, but not for Sepetiba Bay. Our findings
showed trophic magnification factors (TMF) above 1, demonstrating that THg is being
biomagnified up the food chains in Rio de Janeiro bays.
Keywords: tropical ecosystems, food web, stable isotope, heavy metal, bioaccumulation,
Guiana dolphin
1. Introduction
In ecosystems, organisms interact through complex trophic relationships, which
involve energy and nutrient flow between trophic levels. Understanding trophic relationships,
as well as quantitatively assessing trophic levels is of fundamental importance for the
comprehension of ecosystem structure (Lindeman, 1942). In this context, carbon and nitrogen
stable isotope measurements have been successfully used for determinating the potential
sources of primary productivity, as well as for assessing trophic levels in food webs,
respectively (Das et al., 2003a; Fry and Sherr, 1984; Michener and Kaufman, 2007).
Therefore, these measurements provide important information about trophic structure and
energy flow through ecological communities (Cabana and Rasmussen, 1996; Peterson and
Fry, 1987; Vander Zanden et al., 1999). This approach is possible because the stable isotope
composition of a consumer is the weighting average of those of its food source in a predictive
way (DeNiro and Epstein, 1978; Michener and Schell, 1994; Minagawa and Wada, 1984;
Peterson and Fry, 1987).
Some micropollutants, like mercury (Hg), undergo increase in concentrations upward
trophic levels, reaching high concentrations in top-chain organisms (Renzoni et al., 1998).
3
The high potential for Hg biomagnification in aquatic systems is due to the organic form of
the metal (mainly methylmercury – MeHg), which in marine vertebrates accumulates
preferentially muscle (Baeyens et al., 2003; Francesconi and Lenanton, 1992; Wagemann et
al., 1998). With regard to the absorption of mercurial species through the gastrointestinal
tract, MeHg is the most efficiently taken up form of Hg (Wagemann et al., 1998). Therefore,
studying trophic relationships among organisms is also important for a better understating of
contaminant bioaccumulation and biomagnification processes. In this context, several studies
have used nitrogen stable isotopes as indicators of trophic level for investigating contaminant
transfer upward marine food webs (Atwell et al., 1998; Das et al., 2003b; Dehn et al., 2006;
Loseto et al., 2008a; McKinney et al., 2011).
Although there are a number of food web studies dealing with stable isotope ratios and
micropollutant flow, these investigations usually focus on northern hemisphere areas, mainly
in temperate and polar regions (e.g.: Das et al., 2003a; Dehn et al., 2006; Hobson et al., 2002).
In tropical areas, only a few studies have dealt with trophic relationships in estuarine and
marine food webs using stable isotope measurements (Abreu et al., 2006; Corbisier et al.,
2006; Lin et al., 2007). Tropical regions are characterized by high species richness (Begon et
al., 2006), which probably promotes more complex trophic relationships due to greater
diversity of food items for each species (Paine, 1966).
The present study focuses on three different tropical coastal food webs located in a
region under high anthropogenic pressure, the Rio de Janeiro State. Nevertheless, these
environments present different degradation levels. Guanabara Bay is the most degraded area
among the studied bays. The estuary is considered to be the most degraded system of
Brazilian coast (FEEMA, 1990; Kjerfve et al., 1997). Sepetiba Bay presents an intermediate
degree of contamination, but it has undergone a significant increase in pollution over the last
decades (Lacerda et al., 1987; Molisani et al., 2004). Besides, the Sepetiba Bay drainage basin
4
harbors an expanding industrial park (IFIAS, 1998), which can result in worsening of the
degradation scenario. Among the systems considered in the present study, Ilha Grande Bay is
the most preserved one. The estuary is considered to be a biodiversity hotspot and includes a
high number of protected areas (Creed et al., 2007a).
The objectives of the present study were: (1) to investigate the trophic relationships
among organisms from food webs of three tropical coastal ecosystems: Guanabara, Sepetiba
and Ilha Grande bays, (2) to compare the trophic structure from the three food webs
investigated, (3) to calculate the trophic magnification factors (TMF) of total mercury (THg)
between the Guiana dolphin and its prey, and (4) to assess the influence of several factors,
such as the trophic position of the Guiana dolphin, on Hg accumulation.
2. Material and methods
2.1. Sampling
Muscle samples were obtained from Guiana dolphins, Sotalia guianensis, that were
either incidentally captured in gillnet fishery or stranded on the beaches of the three bays of
Rio de Janeiro State between 1995 and 2009: the Guanabara Bay (n = 20), the Sepetiba Bay
(n = 44) and the Ilha Grande Bay (n = 10). All samples were stored at -20 °C until analysis.
The species preyed by S. guianensis were previously identified from stomach content
analysis. They include fish, cephalopod and crustacean species (Azevedo et al., 2008;
Azevedo, unpublished data). Sampling was performed in winter 2008 (August to October –
dry season) and summer 2009 (February and March – wet season). Samples from 34 prey
species (five invertebrate and 29 fish species from distinct feeding habitats) were acquired in
fishing landings inside Guanabara, Sepetiba and Ilha Grande bays (813 individuals). All
specimens were sampled at the body length on which Guiana dolphins prey (Azevedo et al.,
2008; Azevedo, unpublished data). Concerning the scianid fish Micropogonias furnieri, the
5
specimens were sorted out in two groups regarding their length. M. furnieri fitting the size on
which Guiana dolphins exert predation were categorized in group “d”, as well as individuals
larger than 40 cm were placed in group “40”. The specimens were weighed, measured and
dissected. All samples were frozen and stored at -20 °C until analysis.
Seston samples were collected using 75-nm-mesh plankton net in the inner part, at low
tide, as well as in the entrance, at high tide, of each bay. This sampling was carried out in July
2008 (winter) and January 2009 (summer).
2.2. Stable isotope measurements
Stable isotopes measurements of carbon and nitrogen were carried out in muscle
samples from Guiana dolphins, fishes and invertebrates. After being dried at 60 °C (72 h),
samples were ground into a homogeneous powder. Since all muscle samples from the present
study presented low lipid content (C:N < 4.0), no lipid extractions were carried out (Post et
al., 2007). Stable isotope measurements were performed on a V.G. Optima (Isoprime, UK)
isotope ratio mass spectrometer coupled to an N-C-S elemental analyzer (Carlo Erba).
Reference materials (IAEA CH-6 and IAEA-N1) were also analyzed and the precision of
replicate analyses was 0.3‰. Stable isotope ratios are expressed in delta notation as part per
thousand. Carbon and nitrogen ratios are expressed relative to the V-PDB (Vienna Peedee
Belemnite) standard and to atmospheric nitrogen, respectively.
2.3. Total mercury (THg) determination
Aliquots of approximately 0.4 g of muscle (wet weight) were digested with 1mL of
hydrogen peroxide and 5 mL of sulfuric:nitric acid mixture (1:1). The solution was then
heated to 60 °C for 2 hours in a water bath, which was followed by the addition of 5 mL of
potassium permanganate 5% solution and heating to 60 °C for more 15 minutes. After
6
overnight digestion, THg concentration was determined by Cold Vapor/AAS (FIMS-400,
Perkin-Elmer) with sodium borohydride as reducing agent. Blanks were carried through the
procedure in the same way as the sample. The standard reference material DORM-3 (National
Research Council, Canada) was analyzed in every run and our results were in good agreement
with certified values (mean recovery ± SD = 101.44±3.57%).
2.4. Statistical analysis
Mean carbon and nitrogen isotopic values were calculated for Guiana dolphins and for
each prey species. The fish species were classified into five feeding types (see table 1 and 2).
The Kolmogorov-Smirnov test was used in order to test for normality of the data. ANOVA
and post hoc Tukey tests were used for comparing nitrogen and carbon isotopic values among
feeding types (including cephalopod and crustacean species) and among the three bays. The
nonparametric Kruskal-Wallis and post hoc multiple comparison tests were applied when the
data distribution did not follow the rules of normal distribution. The nonparametric MannWhitney U test was performed for comparison between seasons (winter x summer sampling).
Simple linear regression analysis was used for investigating relationships between δ15N and
logarithmic concentrations of THg, as well as for determinating trophic magnification factors
(TMF). TMF is calculated as the antilog of the regression slope with base 10 and can be used
for quantifying food web biomagnification (Borgå et al., 2011; Fisk et al., 2001). Therefore,
this tool was used for calculating Hg biomagnification in different ecosystems.
3. Results and discussion
3.1. Trophic relationships
Summaries of δ13C and δ15N values for cephalopods, crustaceans, fishes and Guiana
dolphins are given in table 1 and 2, respectively, as well in fig. 1.
7
Carbon isotope ratios have proved to be useful in identifying the relative input of
dietary resources from different food webs, as δ13C values are typically higher in species from
coastal or benthic food webs than in those from offshore or pelagic food webs (Hobson, 1999;
McConnaughey and McRoy, 1979). Some fish and cephalopod species were found to be
depleted in 13C in Sepetiba and Guanabara bays (Fig. 1) (from -18.9‰ to -17.1‰ in winter
and from -16.9‰ to -16.3‰ in summer, for Sepetiba Bay; as well as and from -20.8‰ to 17.2‰ in winter and from -19.6‰ to -16.7‰ in summer, for Guanabara Bay). Some of these
species (e.g., Paralonchurus brasiliensis, Cynoscion guatucupa, Umbrina canosai and
Porichthys porosissimus) are marine organisms that use estuaries opportunistically or
optionally during larval, juvenile, sub-adult and even adult stage (Sinque and Muelbert,
1997). Therefore, our findings may be indicating that, for some species, the primary carbon
source is from a neritic food web outside the bays. These findings suggest complex processes
and pointed to the need for detailed investigation for a better understanding of the multiple
sources of carbon in the food webs of Sepetiba and Guanabara bays.
Mean δ13C and δ15N values varied significantly among prey feeding types of Sepetiba
Bay (ANOVA, F6,132 = 15.86 and F6,132 = 72.92 in winter, F6,137 = 14.28 and F6,137 = 50.78 in
summer, p < 0.00001), Guanabara Bay (ANOVA, F6,69 = 9.8 and F6,69 = 5.6 to winter, F6,66 =
16.5 and F6,66 = 3.7 to summer, respectively, p < 0.003) and Ilha Grande Bay food webs
(Kruskal-Wallis test, H = 41.55 and H = 26.88 in winter, H = 40.07 and H = 42.34 in summer,
p < 0.0001). The detritivorous fish Mugil spp. was highly 13C-enriched in Sepetiba (Tukey
HSD test, p < 0.001) and Ilha Grande bays (multiple comparison test, p < 0.01) (fig. 1). These
findings suggest food web inputs of microalgae and/or macroalgae, that are typically higher in
13
C than marine phytoplankton (Boutton, 1991; Fry and Sherr, 1984).
Regarding nitrogen stable isotopes, detritivorous and invertebrate species displayed
the lowest mean δ15N values. Intermediate mean δ15N values were observed in planktivorous
8
and in feeder of benthic invertebrate fishes. Fish and benthic invertebrate feeders as well as
those species of demerso-pelagic feeding habitat showed the highest δ15N values (p < 0.01).
Cephalopod displayed intermediate mean δ15N results in Sepetiba and Guanabara Bays, but
higher δ15N values in Ilha Grande Bay (p < 0.01) (Table 3). These findings followed the usual
food-web nitrogen pattern, in which δ15N values typically show a trophic enrichment between
prey and consumer tissue (Minagawa and Wada, 1984). Consequently, higher trophic position
organisms showed the highest δ15N values, as observed to those species that feed on fishes
(fish and benthic invertebrate feeders and species of demerso-pelagic feeding habitat).
Choloscombrus chrysurus and Trichiurus lepturus are the two demerso-pelagic
species sampled in this study. Stomach content analysis has showed that C. chrysurus prey on
broad taxonomic groups, presenting variable feeding habits among populations (VasconcelosFilho et al., 1984; Carvalho and Soares, 1997; Hofling et al., 1997). The high average δ15N
results suggest fish as an important prey to C. chrysurus in the Rio de Janeiro bays.
Regarding T. lepturus, its diet is composed of pelagic and demersal prey species, especially
fish, associated with estuarine and coastal areas (Bittar et al., 2008; Martins et al., 2005). In
summer sampling, the highest δ15N was verified in T. lepturus (16.61‰), suggesting the
species as the top predator in Sepetiba Bay.
It was expected that Guiana dolphins presented the highest trophic level, but the
average δ15N value for these mammals was lower than those found in several prey species
from Sepetiba (14.0‰) and Ilha Grande bays (14.2‰). On the other hand, in Guanabara Bay,
Guiana dolphin was on the top of the food web, showing the highest mean δ15N value of that
food web. Along the species distribution, stomach analyses have showed different fish species
as preferential prey in distinct Guiana dolphin populations (e.g., Azevedo et al., 2008; Di
Beneditto and Ramos, 2004; Gurjão et al., 2003). In fact, our findings suggest that Guiana
dolphin feeds on organisms that occupy distinct trophic levels among the three bays studied
9
here. In Sepetiba and Ilha Grande bays, Guiana dolphin probably feeds on organisms that
occupy relatively lower trophic levels than in Guanabara Bay.
3.2. Comparison among bays
The carbon and nitrogen isotopic findings pointed to different trophic relationships in
the food webs of Sepetiba, Guanabara and Ilha Grande bays. The three studied bays are under
anthropogenic pressure, but in different degradation levels. As mentioned, Guanabara Bay is
the most degraded estuary among the three studied bays. In fact, it is considered to be one of
the most degraded systems of Brazilian coast (FEEMA, 1990; Kjerfve et al., 1997). The
Guanabara Bay food web showed less complex trophic relationships than did Sepetiba and
Ilha Grande bays. In Sepetiba and Ilha Grande bays the trophic relationships among the fish
species were not well defined and the systems seem to be complex, as it is expected for
tropical food webs. The high biodiversity found in these systems probably promotes great
variety of prey for each predator (Paine, 1966). Concerning fish and benthic invertebrate
feeders and demerso-pelagic species from Sepetiba and Ilha Grande bays, it was not possible
to determine specific groups of prey through nitrogen isotopic values. This finding suggests
that these species are preying on several different taxa.
Ilha Grande Bay showed significant depleted δ13C values for all feeding types (except
for detritivorous species), as well as for Guiana dolphins, compared to Guanabara and
Sepetiba bays both in winter and summer season (Tukey HSD test, p < 0.05) (Table 1 and 4).
Ilha Grande Bay is not a confined estuary like the other two bays. In addition to this feature,
this body of water receive colder and more saline water by marine current flow from
continental shelf than the other bays considered herewith (Signorini, 1980a,b). Therefore, the
carbon isotopic values probably reflect higher marine influence in Ilha Grande Bay than in
Guanabara and Sepetiba bays.
10
Planktivorous and benthic invertebrate feeder fishes from Sepetiba and Ilha Grande
bays showed higher δ15N values than those feeding type groups from Guanabara Bay in the
winter season (Kruskal-Wallis test, H = 26.68 and H = 47.24, respectively, p < 0.0001). These
values ranged from 11.5‰ to 15.8‰ for Sepetiba Bay and from 12.5‰ to 15.6‰ for Ilha
Grande Bay. In Guanabara Bay, the nitrogen isotopic values ranged from 7.4‰ to 13.3‰ for
these two feeding types. Additionally, Sepetiba Bay showed the highest δ15N for fish and
benthic invertebrate feeders (from 13.7‰ to 16.7‰ in winter and from 13.7‰ to 16.8‰ in
summer) and for those species of demerso-pelagic feeding habit (from 15.5‰ to 16.5‰ in
winter and from 15.2‰ to 17.1‰ in summer) (multiple comparison test, p < 0.0012). Since
δ15N values can vary from system to system even when the same species is considered
(Cabana and Rasmussen, 1996), caution should be taken when comparing δ15N values
between food webs.
Several studies have reported more δ15N-enriched values in organisms from areas
undergoing eutrophication process due to city sewage, effluents of industries and agricultural
fertilizers (Abreu et al., 2006; McClelland and Valiela, 1998; Olsen et al., 2010).
Interestingly, Guanabara Bay, the most eutrophicated system among the three sampled areas,
showed depleted δ15N values compared to both Sepetiba and Ilha Grande bays. Phytoplankton
in Guanabara Bay is dominated by nanoplanktonic and cyanobacteria species (Valentin et al.,
1999). Therefore, our findings may be reflecting a substantial input of atmospheric nitrogen
fixation by cyanobacteria, which results in low δ15N values (Carpenter et al., 1997;
McClelland et al., 2003). In contrast, Kalas et al. (2009) found enriched δ15N values in
particulate organic matter from Guanabara Bay. The authors suggested it could be due to the
incorporation of isotopically heavy residual NH4+ by the phytoplankton. However, the
sampling was performed in 1999 and 2000. The distinct results obtained through this 10-year
interval between the investigation carried out by Kalas et al. (2009) and the present study may
11
suggest worsening in the Guanabara Bay degradation process over the time. The presence of
cyanobacteria is usually associated to the eutrophication process. The fact that organism from
Guanabara Bay food web present relatively low nitrogen isotopic values probably reflects
elevated cyanobacteria density in this estuary. These findings point out an accelerated
eutrophication process that indicates a much higher degradation condition in Guanabara Bay
than it could be assumed previously.
3.3. THg-δ15N relationships
Average muscular total mercury concentration (THg) was lowest in Litopenaeus.
schmitt (3.6 ng/g in Guanabara Baywinter and 4.2 ng/g in Sepetiba Baywinter) and in Sardinella
brasiliensis (4.6 ng/g in Ilha Grande Baywinter) and highest in Guiana dolphin (920.3 ng/g in
Guanabara Bay, 269.2 ng/g in Sepetiba Bay and 688.4 ng/g in Ilha Grande Bay) (Table 5).
THg concentrations in prey species increased successively with increasing trophic level in
Guanabara, Sepetiba and Ilha Grande bays, except for those species of demerso-pelagic
feeding habitat. Detritivorous and invertebrate species displayed the lowest mean δ15N values
as well as the lowest THg concentrations, while fish and benthic invertebrate feeders showed
the highest mean δ15N values and THg concentrations (Kuskal-Wallis test, p < 0.0009).
However, demerso-pelagic species present equivalent high δ15N values, but their THg
concentrations were intermediate.
A positive linear relationship was found between log-transformed concentrations of
THg and δ15N values for Guanabara and Ilha Grande bays (linear regression, p < 0.005), and
was just above the significance level at Sepetiba Bay (linear regression, p > 0.06) (Fig.2).
Trophic magnification factors (TMF) were above 1 (Table 6), which indicates mercury
accumulation in the food web and suggests diet as the major exposure route for this element
(Borgå et al., 2011; Gray, 2002) in these bays. Muscular mercury in fish and marine mammals
12
exists predominantly in organic forms, which are efficiently incorporated by food intake
(Francesconi and Lenanton, 1992; Wagemann et al., 1998).
The TMF values for Guanabara and Ilha Grande bays (1.51–1.67) were similar to
those observed in arctic marine food web (1.59 – value converted from slope of the regression
to TMF for comparison to our results) by Atwell et al. (1998) and in Gulf of St. Lawrence
(1.48 – value converted) by Lavoie et al. (2010). They are slightly lower than those reported
for three food webs from Beaufort Sea (ca. 1.8 – value converted) by Loseto et al. (2008a).
For Alaskan Arctic region, Dehn et al. (2006) found an extremely high TMF value (25.12 –
value converted). Differently from Atwell et al. (1998), Loseto et al. (2008a), Lavoie et al.
(2010) and the present study, the investigation performed by Dehn et al. (2006) focused
largely on marine mammals rather than on overall mercury biomagnification through many
taxonomic groups. Unbalanced study designs that include large numbers of high trophic level
species, as in the investigation performed by Dehn et al. (2006), may affect the TMF results,
so that TMF values can reflect biomagnification at these higher trophic levels rather than at
full food web (Borgå et al., 2011).
Conversely, aspects other than biomagnification may be influencing mercury
bioaccumulation in some species from Rio de Janeiro bays. This is especially evident in
Sepetiba Bay, where a linear relationship between log THg concentrations and δ15N values
was not observed. Guiana dolphin showed the highest mean mercury concentration (269.23
ng/g) for Sepetiba Bay, but not the highest δ15N values. This finding may be associated to
bioaccumulation over the time as well as to a great body mass, which requires a higher food
intake by the species. There is little evidence that THg accumulates in muscle tissue with age
in cetaceans (Atwell et al., 1998; Loseto et al., 2008b), but positive relationship between THg
and body length was found (Loseto et al., 2008b).
13
Regarding most fish species and Guiana dolphins, higher THg concentrations were
found in Guanabara and Ilha Grande bays than in Sepetiba Bay (p<0.05). Ilha Grande and
Sepetiba bays are adjacent bodies of water that are connected to each other by a channel.
Sepetiba Bay receives a substantial input of Hg from effluents of industries and cities located
in its drainage basin, as well as from transposition of Paraíba do Sul River (Molisani et al.,
2007). Several studies investigated the behavior of Hg in the latter bay and it was observed
that a high percentage of the bioavailable Hg is transported to adjacent areas, such as Ilha
Grande Bay and continental shelf waters. This transport would occur due to the high Hgcomplexing capacity demonstrated by the dissolved organic matter (Lacerda and Malm, 2008;
Molisani et al., 2007). The fact that higher THg concentrations were found in Ilha Grande Bay
than in Sepetiba Bay (present study; Marins et al., 1998) suggests a lower bioavailability in
the latter body of water (Lacerda and Malm, 2008). This low bioavailability of THg in
Sepetiba Bay may reflect in lower trophic transfer efficiency, explaining the lack of a linear
relationship between log THg concentrations and δ15N values in Sepetiba Bay food web.
It is important to emphasize that the THg concentrations in biota from Ilha Grande
Bay are not only higher than in organisms from Sepetiba Bay but also comparable to the THg
levels in biota from Guanabara Bay. This finding may be a result of two factors: (1) the South
Atlantic Central Water (SACW) influence over Ilha Grande Bay, as well as (2) partial
transport of Hg complexed to organic matter from Guanabara Bay to continental shelf waters.
Regarding the first aspect , it is important to mention that the SACW is considered to be a
significant source of Hg to the continental shelf via upwelling (Cossa et al., 1996; Mason and
Fitzgerald, 1993). Advection by upwelling is an example of a physical transport process with
important implications in organic compound redistribution, especially for nektonic organisms
(Dorneles et al., 2010). The SACW reach the superficial water during the summer and its
influence over the southeast Brazilian region is well-know (Brandini et al., 1997), including
14
the Ilha Grande Bay (Creed et al., 2007b). Concerning the second factor, it becomes
interesting to consider that , in many estuaries, a significant percentage of the received Hg
burden is exported from the body of water after being complexed to the organic matter
(Kremling, 1988). Besides, it was observed that the eutrophication conditions of Guanabara
Bay influences the bioavailability of Hg to organisms, promoting a decrease in its trophic
transfer efficiency through the food web of that estuarine system (Kehrig et al., 2009).
The distinct TMF values found for the three food webs could be associated to the
differences in THg bioavailability in each bay. The highest TMF value verified in the Ilha
Grande Bay food web is likely to be a consequence of a higher percentage of bioavailable Hg
in this estuary than in Sepetiba Bay or in Guanabara Bay. Although Ilha Grande Bay is the
most preserved system among those considered herewith, our findings suggest that the highest
THg trophic transfer efficiency observed in its food web results in higher THg concentrations
in organisms from that Bay.
4. Conclusions
Carbon and nitrogen isotopic findings revealed different trophic relationships in the
food webs of Sepetiba, Guanabara and Ilha Grande bays. Variations in the THg
biomagnification processes among the three food webs suggest that particular characteristics
of each area are more likely to affect the TMF than the Hg burden received by each bay.
Nitrogen isotopic values were successfully used for investigating trophic relationships and
hence trophic magnification of Hg in the studied food webs. More studies are needed to
explain variations in the trophic transfer of Hg in each bay, as well as among the food webs.
Acknowledgments
15
This work was supported by Rio de Janeiro State Government Research Agency –
FAPERJ (“Pensa Rio” Program - Proc. E-26/110.371/2007), Ministry of Education of Brazil
– CAPES (“Ciencias do Mar” - Proc. 23038.051661/2009-18), Brazilian Research Council –
CNPq (Proc. 482938/2007-2 and Proc. 480701/2009-1) and Cetacean Society International
grant. TL Bisi has a scholarship from the Ministry of Education of Brazil – CAPES, J
Lailson-Brito has a research grant from FAPERJ/UERJ (“Prociência” Program) and CNPq
(grant #305303/2010-4), AF Azevedo has a research grant from CNPq (grant #304826/20081) and FAPERJ (JCNE #101.449/2010). G Lepoint and K Das are F.R.S. - FNRS Research
Associates. We thank to Aquatic Mammal and Bioindicator Laboratory (MAQUA/UERJ)
team for invaluable assistance in sampling, as well as in sample preparation for stable
isotopes and total mercury determination. We particularly thank to Adriana Nascimento
Gomes, Sylvia Chada, Regis Pinto de Lima and José Carlos from Estação Ecológica Tamoios
(ESEC Tamoios-ICMBio) for logistical support in Ilha Grande Bay. We also thank two
anonymous reviewers who made useful suggestions that have helped to improve the
manuscript.
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24
Table 1. Mean δ13C values (‰) ± SD and number of individuals (n) of seston, cephalopods,
crustaceans, fishes and Guiana dolphin from Guanabara, Sepetiba and Ilha Grande bays, Rio
de Janeiro State.
Species
Seston
Inner
Entrance
Cephalopods
Loliginidae
Loligo plei
Guanabara Bay
winter
Summer
Sepetiba Bay
winter
summer
Ilha Grande Bay
winter
summer
-19.4
-18.5
-19.0
n.d.
-19.0
-16.6
-14.6
-18.2
-22.5
-20.6
-18.9±0.5
(n=6)
-16.1±0.1
(n=3)
-18.2±0.3
(n=7)
Loligo sanpaulensis
Lolliguncula brevis
-17.1±1.1
(n=10)
Crustaceans
Penaeidae
Farfantepenaeus brasiliensis
Litopenaeus schmitt
-15.6±0.6
(n=6)
-15.2±0.2
(n=3)
Fishes
Ariidae
Aspistor luniscutisa
Batrachoididae
Porichthys porosissimusb
Carangidae
Chloroscombrus chrysurusc
Centropomidae
Centropomus spp.b
Clupeidae
Sardinella brasiliensisd
Engraulididae
Anchoa spp.d
Cetengraulis edentulusd
-15.4±1.4
(n=6)
-13.2±0.2
(n=6)
-18.8±0.8
(n=5)
-15.1±0.5
(n=5)
-14.7±0.6
(n=6)
-14.9±0.4
(n=6)
-20.9±1.3
(n=6)
-14.3±0.1
(n=3)
-15.6±0.4
(n=6)
-19.6±0.6
(n=6)
-15.9±0.3
(n=6)
-14.1±0.5
(n=6)
-15.1±0.3
(n=6)
-14.8±0.6
(n=6)
Mugilidae
Mugil curema e
Mugil Liza e
Mugil spp.e
Paralichthydae
-14.4±0.9
(n=5)
-17.8±0.7
(n=5)
-17.6±0.7
(n=6)
-18.9±0.0
(n=3)
-18.5±0.4
(n=6)
-13.1±0.4
(n=6)
-17.6±0.2
(n=6)
-16.6±0.5
(n=6)
-14.3±1.1
(n=6)
-14.7±1.6
(n=6)
-15.8±0.7
(n=6)
-16.8±0.2
(n=3)
-16.3±0.6
(n=6)
-15.2±0.6
(n=6)
-15.7±0.1
(n=5)
-18.3±1.0
(n=6)
-15.2±0.3
(n=6)
-14.2±0.6
(n=3)
-14.9±0.2
(n=6)
-15.7±0.6
(n=4)
-14.1±0.4
(n=6)
-14.4±0.5
(n=6)
-14.9±0.2
(n=6)
-14.2±0.9
(n=6)
-13.8±0.5
(n=6)
-9.4±1.4
(n=4)
-13.9±1.0
(n=6)
-11.1±0.9
(n=5)
Engraulis anchoitad
Haemulidae
Orthopristis rubera
-15.9±0.5
(n=5)
-14.5±1.1
(n=4)
-15.1±0.9
(n=5)
-14.0±0.8
(n=5)
-17.6±0.5
(n=3)
Cynoglossidae
Symphurus tesselatusa
-18.6±0.3
(n=6)
-15.3±0.7
(n=5)
-14.3±0.2
(n=5)
-18.9±0.5
(n=5)
-19.4
-18.5
-16.7±0.5
(n=6)
-10.9±1.4
(n=5)
-10.6±1.1
(n=6)
25
Paralichthys patagonicusa
-18.03±0.5
(n=4)
Sciaenidae
Ctenosciaena gracilicirrhusa
Cynoscion guatucupa b
Cynoscion jamaicensisb
Cynoscion leiarchusb
-17.2
(n=1)
-18.9±0.3
(n=6)
-16.3±0.1
(n=5)
-17.0±0.8
(n=6)
-15.8±0.9
(n=6)
-13.9±0.4
(n=6)
Isopisthus parviponnisb
Larimus brevicepsb
-17.7±0.7
(n=6)
Menticirrhus americanusa
Micropogonias furnieri “d”a
Micropogonias furnieri “40”b
Paralonchurus brasiliensisa
-16.3±0.8
(n=14)
-16.1±1.4
(n=7)
-17.8±0.7
(n=6)
-16.2±1.0
(n=13)
-15.4±1.6
(n=7)
-16.7±0.4
(n=6)
Stellifer rastriferb
Stellifer stelliferb
Umbrina canosaia
Sparidae
Pagrus pagrus c
-14.4±0.6
(n=6)
-13.4±1.4
(n=13)
-14.3±2.0
(n=6)
-14.0±0.3
(n=6)
-14.4±0.2
(n=5)
-13.9
(n=1)
-16.7±0.8
(n=5)
-18.0±0.7
(n=6)
-17.7±0.3
(n=6)
-16.2±0.7
(n=6)
-16.5±0.6
(n=6)
-16.5±1.2
(n=14)
-16.6±0.4
(n=10)
-17.0±0.8
(n=6)
-17.1±0.5
(n=3)
-18.5±0.2
(n=2)
-17.7±0.2
(n=6)
-16.2±0.7
(n=13)
-16.3±0.9
(n=8)
-16.3±0.3
(n=6)
-16.3±0.3
(n=2)
-15.6±0.0
(n=2)
-15.9±0.2
(n=6)
-15.0±0.5
(n=6)
-18.5±0.4
(n=6)
-18.7±0.3
(n=6)
-18.9±0.7
(n=6)
-16.9±0.2
(n=6)
-18.2±0.2
(n=6)
-17.3±0.2
(n=6)
-17.2±0.8
(n=5)
-13.8±0.5
(n=6)
-17.8±0.1
(n=5)
-17.4±0.7
(n=5)
-14.0±0.7
(n=20)
n.d. – not determined.
blank – not analyzed.
a
Fish feeding type: benthic invertebrate feeder.
b
Fish feeding type: fish and benthic invertebrate feeder.
c
Fish feeding type: demerso-pelagic predator.
d
Fish feeding type: planktivorous.
e
Fish feeding type: detritivorous.
-14.5±1.0
(n=44)
-14.5±0.4
(n=2)
-15.1±0.4
(n=6)
-17.9±0.1
(n=6)
-14.2±0.2
(n=6)
-15.1
(n=1)
Trichiuridae
Trichiurus lepturusc
Cetacea
Sotalia guianensis
-12.6±1.1
(n=5)
-15.3±0.6
(n=6)
-15.34±0.7
(n=6)
-12.8±0.4
(n=4)
-13.8±1.7
(n=13)
-14.7±1.4
(n=7)
-15.5±0.7
(n=5)
-15.1±0.1
(n=3)
-14.4±0.1
(n=3)
-14.5±0.3
(n=6)
-16.3
(n=1)
-15.6±1.1
(n=6)
-14.0±0.6
(n=6)
-14.2±0.4
(n=6)
-17.6±0.1
(n=6)
Serranidae
Diplectrum radialea
Serranus aurigaa
-19.2±0.3
(n=4)
-17.1±0.4
(n=6)
-16.6±0.4
(n=10)
26
Table 2. Mean δ15N values (‰) ± SD and number of individuals (n) of seston, cephalopods,
crustaceans, fishes and Guiana dolphins from Guanabara, Sepetiba and Ilha Grande bays, Rio
de Janeiro State.
Species
Seston
Inner
Entrance
Cephalopods
Loliginidae
Loligo plei
Guanabara Bay
winter
summer
n.d.
n.d.
n.d.
n.d.
n.d.
7.6
12.4±0.8
(n=6)
15.5±0.1
(n=3)
13.9±0.6
(n=7)
Loligo sanpaulensis
Lolliguncula brevis
11.9±1.2
(n=10)
Crustaceans
Penaeidae
Farfantepenaeus brasiliensis
Litopenaeus schmitt
8.7±2.3
(n=6)
10.8±1.2
(n=3)
Fishes
Ariidae
Aspistor luniscutisa
Batrachoididae
Porichthys porosissimusb
Carangidae
Chloroscombrus chrysurusc
Centropomidae
Centropomus spp.b
Clupeidae
Sardinella brasiliensisd
14.1±0.3
(n=6)
15.9±0.3
(n=6)
13.6±0.9
(n=6)
13.2±0.8
(n=3)
10.5±0.2
(n=6)
10.5±0.3
(n=6)
Cetengraulis edentulusd
Mugilidae
Mugil curema e
Mugil Liza e
Mugil spp.e
Paralichthydae
Paralichthys patagonicusa
10.40±1.45
(n=5)
9.3±2.1
(n=5)
7.1
n.d.
14.5±0.7
(n=6)
12.5±0.2
(n=3)
12.6±0.1
(n=6)
15.6±0.3
(n=6)
14.1±0.3
(n=6)
14.6±0.3
(n=6)
15.3±0.9
(n=6)
15.1±0.9
(n=6)
13.7±0.8
(n=6)
14.9±0.3
(n=3)
13.0±0.3
(n=6)
13.3±0.2
(n=6)
13.2±0.5
(n=5)
11.6±0.4
(n=6)
14.2±0.7
(n=6)
14.3±1.2
(n=3)
14.6±0.3
(n=6)
13.8±0.1
(n=4)
14.9±0.53
(n=6)
14.3±0.4
(n=6)
15.1±0.1
(n=6)
15.1±0.2
(n=6)
14.6±1.3
(n=6)
9.2±0.3
(n=4)
9.6±0.8
(n=6)
10.0±0.8
(n=5)
Engraulis anchoitad
Haemulidae
Orthopristis rubera
n.d.
n.d.
14.2±0.4
(n=5)
15.2±0.8
(n=4)
14.5±0.7
(n=6)
13.3±2.2
(n=5)
Ilha Grande Bay
winter
summer
14.0±0.4
(n=6)
13.9±1.2
(n=6)
12.8±0.3
(n=5)
13.4±0.5
(n=6)
11.1±2.2
(n=6)
8.9
8.3
11.8±0.9
(n=5)
11.3±0.6
(n=5)
12.7±0.0
(n=3)
12.3±0.7
(n=6)
11.0±0.8
(n=6)
summer
12.2±0.4
(n=5)
11.6±0.9
(n=5)
12.1±0.2
(n=5)
Cynoglossidae
Symphurus tesselatusa
Engraulididae
Anchoa spp.d
Sepetiba Bay
winter
12.1±0.4
(n=6)
9.4±0.7
(n=5)
13.2±0.5
8.8±1.3
(n=6)
27
(n=4)
Sciaenidae
Ctenosciaena gracilicirrhusa
Cynoscion guatucupa b
Cynoscion jamaicensisb
Cynoscion leiarchusb
15.7
(n=1)
14.2±0.1
(n=6)
9.6±0.4
(n=5)
13.9±0.2
(n=6)
13.9±0.3
(n=6)
12.7±1.1
(n=6)
Isopisthus parviponnisb
Larimus brevicepsb
14.8±0.5
(n=6)
Menticirrhus americanusa
Micropogonias furnieri “d”a
Micropogonias furnieri “40”b
Paralonchurus brasiliensisa
10.3±1.6
(n=14)
13.9±0.8
(n=7)
14.5±0.6
(n=6)
11.3±1.9
(n=13)
12.4±2.09
(n=7)
14.2±0.6
(n=6)
Stellifer rastriferb
Stellifer stelliferb
Umbrina canosaia
Sparidae
Pagrus pagrusc
14.9±0.9
(n=6)
13.4±1.1
(n=13)
14.6±0.86
(n=6)
14.9±0.3
(n=6)
15.9±0.4
(n=5)
15.817
(n=1)
13.4±0.2
(n=5)
14.3±0.3
(n=6)
13.9±0.2
(n=6)
14.8±0.5
(n=6)
14.5±0.9
(n=6)
14.1±0.8
(n=14)
14.7±0.5
(n=10)
13.6±0.6
(n=6)
14.3±0.5
(n=3)
13.63±0.08
(n=2)
13.7±0.3
(n=6)
13.8±0.9
(n=13)
14.6±0.5
(n=8)
13.6±0.7
(n=6)
14.1±0.1
(n=2)
14.2±0.0
(n=2)
11.4±1.3
(n=6)
13.5±0.3
(n=6)
12.9±0.2
(n=6)
12.1±0.8
(n=6)
13.1±0.6
(n=6)
14.1±0.2
(n=6)
13.6±0.2
(n=6)
14.2±0.2
(n=6)
14.9±0.8
(n=5)
16.6±0.4
(n=6)
14.6±0.4
(n=5)
14.2±0.3
(n=5)
14.2±0.9
(n=20)
n.d. – not determined.
blank – not analyzed.
a
Fish feeding type: benthic invertebrate feeder.
b
Fish feeding type: fish and benthic invertebrate feeder.
c
Fish feeding type: demerso-pelagic predator.
d
Fish feeding type: planktivorous.
e
Fish feeding type: detritivorous.
14.0±0.6
(n=44)
14.3±0.2
(n=2)
13.2±0.3
(n=6)
14.2±0.2
(n=6)
14.9±0.3
(n=6)
14.3
(n=1)
Trichiuridae
Trichiurus lepturusc
Cetacea
Sotalia guianensis
15.9±0.2
(n=5)
15.8±0.3
(n=6)
15.8±0.5
(n=6)
13.1±1.5
(n=4)
13.2±1.1
(n=13)
15.0±0.73
(n=7)
14.8±0.3
(n=5)
15.4±0.3
(n=3)
16.3±0.0
(n=3)
14.9±0.4
(n=6)
13.9
(n=1)
14.3±0.8
(n=6)
15.1±0.5
(n=6)
16.06±0.43
(n=6)
13.9±0.4
(n=6)
Serranidae
Diplectrum radialea
Serranus aurigaa
15.7±0.2
(n=4)
14.3±0.2
(n=6)
14.2±0.6
(n=10)
28
Table 3. Mean δ15N values (‰) of invertebrate species, cephalopods, benthic invertebrate
feeder, fish and benthic invertebrate feeder, demerso-pelagic predator, planktivorous and
detritivorous from Guanabara, Sepetiba and Ilha Grande bays, Rio de Janeiro State.
Invertebrates
Detritivorous
Planktivorous
Benthic invertebrate feeder
Fish and benthic
invertebrate feeder
Demerso-pelagic predator
Cephalopods
Guanabara Bay
winter
summer
8.7
10.7
9.3
10.4
11.3
12.3
10.7
12.3
Sepetiba Bay
winter
summer
11.9
11.4
9.4
10.3
13.8
14.7
14.2
14.2
Ilha Grande Bay
winter
summer
9.4
8.8
13.2
11.6
13.8
13.3
12.1
13.0
15.6
15.3
14.2
14.5
13.3
11.9
14.1
12.4
15.9
14.4
16.1
14.6
14.1
14.0
14.3
14.5
29
Table 4. Mean δ13C values (‰) of invertebrate species, cephalopods, benthic invertebrate
feeder, fish and benthic invertebrate feeder, demerso-pelagic predator, planktivorous and
detritivorous from Guanabara, Sepetiba and Ilha Grande bays, Rio de Janeiro State.
Invertebrates
Detritivorous
Planktivorous
Benthic invertebrate feeder
Fish and benthic
invertebrate feeder
Demerso-pelagic predator
Cephalopods
Guanabara Bay
winter
summer
-15.6
-15.2
-17.8
-14.4
-15.2
-14.9
-16.2
-15.8
Sepetiba Bay
winter
summer
-14.8
-14.6
-12.1
-11.1
-15.6
-14.7
-14.5
-14.0
Ilha Grande Bay
winter
summer
-10.9
-10.6
-15.7
-18.2
-17.0
-16.3
-16.1
-14.9
-14.6
-14.3
-17.1
-16.5
-15.1
-17.1
-14.7
-18.9
-14.9
-17.6
-13.3
-15.3
-17.9
-18.6
-17.1
-17.6
30
Table 5. Mean muscular total mercury (THg) concentration (ng/g) ± SD and number of
individuals (n) cephalopods, crustaceans, fishes and Guiana dolphins from Guanabara,
Sepetiba and Ilha Grande bays, Rio de Janeiro State.a
Species
Guanabara Bay
winter
summer
Sepetiba Bay
winter
summer
Cephalopoda
Loliginidae
Loligo plei
Ilha Grande Bay
winter
summer
21.18±7.3
(n=6)
Loligo sanpaulensis
Lolliguncula brevis
Crustacea
Penaeidae
Litopenaeus schmitti
12.3±4.1
(n=6)
36.3±21.1
(n=9)
12.9±7.0
(n=4)
3.6±1.8
(n=6)
Fishes
Ariidae
Aspistor luniscutis
4.2±2.1
(n=6)
6.5±1.5
(n=5)
24.2±26.1
(n=6)
8.5±2.7
(n=6)
Batrachoididae
Porichthys porosissimus
Carangidae
Chloroscombrus chrysurus
20.2±7.1
(n=5)
Centropomidae
Centropomus spp.
Clupeidae
Sardinella brasiliensis
31.2±16.1
(n=6)
19.0±9.3
(n=6)
99.5±61.7
(n=6)
51.8±16.4
(n=6)
65.7±22.1
(n=3)
33.5±23.1
(n=6)
44.7±9.9
(n=6)
80.7±38.7
(n=6)
169.0±21.4
(n=3)
5.0±2.0
(n=6)
5.8±0.8
(n=6)
4.6±1.1
(n=6)
20.5±6.6
(n=6)
4.4±2.2
(n=6)
8.3±2.9
(n=3)
29.8±7.1
(n=6)
7.8±4.5
(n=4)
32.6±12.2
(n=6)
8.0±0.8
(n=6)
59.6±7.1
(n=6)
15.8±10.6
(n=6)
15.4±6.9
(n=6)
27.8±6.3
(n=6)
Cetengraulis edentulus
93.1±50.4
(n=6)
15.4±8.1
(n=6)
43.4±8.0
(n=6)
27.9±9.6
(n=6)
Engraulis anchoita
Haemulidae
Orthopristis ruber
Mugilidae
Mugil liza
Mugil spp.
Cynoscion guatucupa
7.6±1.4
(n=5)
12.1±3.6
(n=5)
6.7±1.3
(n=5)
Paralichthydae
Paralichthys patagonicus
Sciaenidae
Ctenosciaena gracilicirrhus
28.3±7.8
(n=5)
44.77±16.4
(n=4)
Cynoglossidae
Symphurus tesselatus
Engraulididae
Anchoa spp.
62.9±29.8
(n=3)
18.2±1.6
(n=4)
12.7±7.0
(n=4)
18.2±2.7
(n=6)
41.7±9.5
19.6±5.0
31
(n=6)
Cynoscion jamaicensis
Cynoscion leiarchus
66.9±9.8
(n=4)
54.9±39.4
(n=6)
44.3±8.7
(n=6)
Isopisthus parvipinnis
Larimus breviceps
Menticirrhus americanus
Micropogonias furnieri “d”
Micropogonias furnieri “40”
83.4±107.9
(n=14)
252.7±214.5
(n=7)
23.8±23.4
(n=13)
111.2±46.4
(n=7)
Paralonchurus brasiliensis
Stellifer rastrifer
Stellifer stellifer
27.5±5.0
(n=5)
12.5±6.8
(n=6)
16.8±8.04
(n=6)
10.5±7.5
(n=4)
7.1±6.5
(n=12)
107.6±134.0
(n=7)
10.46±6.0
(n=5)
6.1±1.3
(n=3)
14.5±3.7
(n=3)
47.0±30.2
(n=6)
24.4±14.1
(n=6)
44.9±10.8
(n=6)
19.93±8.40
(n=6)
7.46±5.9
(n=12)
135.5±99.5
(n=5)
5.8±1.5
(n=6)
19.4±10.2
(n=5)
24.4
(n=1)
Umbrina canosai
Serranidae
Diplectrum radiale
Serranus auriga
66.5±23.9
(n=6)
90.3±21.3
(n=6)
15.8±7.3
(n=6)
9.5
(n=1)
Cetacea
Sotalia guianensis
36.3±9.5
(n=6)
920.3±656.2
(n=12)
269.2±332.3
(n=42)
Blank – not analyzed.
a
Total mercury determination was not carried out in species that were depleted in 13C.
44.0±37.4
(n=6)
33.1±33.4
(n=11)
264.0±96.8
(n=10)
16.9±5.0
(n=6)
26.4±15.6
(n=2)
24.0±10.9
(n=3)
126.5±31.1
(n=6)
49.7±43.2
(n=13)
226.1±126
(n=7)
13.8±2.9
(n=6)
38.8±4.1
(n=2)
53.5±16.7
(n=2)
39.2±12.1
(n=6)
34.8±5.9
(n=6)
37.1±12.8
(n=5)
22.5±17.1
(n=5)
20.4±0.2
(n=2)
12.5±1.2
(n=6)
Sparidae
Pagrus pagrus
Trichiuridae
Trichiurus lepturus
49.3±18.7
(n=5)
70.4±34.3
(n=6)
(n=6)
27.8±7.4
(n=6)
688.4±221.8
(n=9)
32
Table 6. Trophic Magnification factors (TMF) and simple linear regression values among log
of THg concentration and δ15N value to Sepetiba, Guanabara and Ilha Grande bays food webs,
Rio de Janeiro Coast.
Sepetiba Baywinter
Sepetiba Baysummer
Guanabara Baywinter
Guanabara Baysummer
Ilha Grande Bay winter
Ilha Grande Baysummer
n
155
175
86
74
105
100
slope
0.07
0.07
0.19
0.18
0.21
0.22
SEslope
0.04
0.04
0.03
0.03
0.07
0.05
TMF
1.19
1.17
1.55
1.51
1.63
1.67
intercept
0.31
0.46
-0.52
-0.51
-1.22
-1.50
R2
0.02
0.02
0.36
0.30
0.07
0.19
p-value
0.0942
0.0665
0.0001
0.0001
0.0053
0.0001
33
18
18
Sepetiba Bay
winter
Sepetiba Bay
summer
16
16
14
15N (‰)
15N (‰)
14
12
10
12
10
8
8
6
-20
-18
-16
-14
-12
-10
6
-8
-20
-18
-16
13C (‰)
-12
-10
18
18
Guanabara Bay
summer
Guanabara Bay
winter
16
16
14
14
15N (‰)
15N (‰)
-14
13C (‰)
12
12
10
10
8
8
6
6
-21
-22
-20
-18
-16
-14
-20
-19
-12
-18
-17
-16
-15
-14
-13
13C (‰)
13C (‰)
18
18
Ilha Grande Bay
winter
Ilha Grande Bay
summer
16
16
15N (‰)
15N (‰)
14
14
12
12
10
8
10
6
8
-20
-22
-20
-18
-16
13C (‰)
-14
-12
-10
-18
-16
-14
-12
-10
13C (‰)
Fig. 1. Trophic structure of Sepetiba, Guanabara and Ilha Grande bays food webs as
determinate from stable isotope carbon and nitrogen ratios (mean±SE). seston,
crustacean, cephalopod, detritivorous, planktivorous, benthic invertebrate feeder,
invertebrate feeders, demerso-pelagic, Guiana dolphin.
fish and benthic
34
3,5
3,5
Sepetiba Bay
winter
3,0
Sepetiba Bay
summer
3,0
15
Log 10 [Hg] = 0.07(15N) +0.46
Log 10 [Hg] = 0.07( N) + 0.31
2,5
Log10 [THg] ng/g
Log10 [THg] ng/g
2,5
2,0
1,5
1,0
2,0
1,5
1,0
0,5
0,5
0,0
0,0
-0,5
8
10
12
14
16
18
8
10
12
 N (‰)
15
14
16
18
15N (‰)
4,0
4,0
Guanabara Bay
winter
3,5
Guanabara Bay
summer
3,5
Log 10 [Hg] = 0.19( 15 N) – 0,52
Log 10 [Hg] = 0.18( 15 N) – 0,51
Log10 [THg] ng/g
Log10 [THg] ng/g
3,0
2,5
2,0
1,5
1,0
0,5
3,0
2,5
2,0
1,5
1,0
0,0
6
8
10
12
14
16
0,5
18
6
 N (‰)
15
12
14
16
18
3,5
Ilha Grande Bay
winter
Ilha Grande Bay
summer
3,0
Log 10 [Hg] = 0.21( 15 N) – 1,22
Log 10 [Hg] = 0.22( 15 N) – 1.50
2,5
Log10 [THg] ng/g
Log10 [THg] ng/g
10
15N (‰)
3,5
3,0
8
2,0
1,5
1,0
0,5
0,0
12,0
2,5
2,0
1,5
1,0
12,5
13,0
13,5
14,0
14,5
15,0
15,5
 N (‰)
15
16,0
0,5
10
11
12
13
14
15
16
17
15N (‰)
Fig. 2. Relationship between δ15N values and log-transformed concentrations of total mercury
(THg) in organisms from the Sepetiba, Guanabara and Ilha Grande bays food webs, Rio de
Janeiro Coast. crustacean, cephalopod, detritivorous, planktivorous, benthic invertebrate
feeder,
fish and benthic invertebrate feeders,
demerso-pelagic,
Guiana dolphin